Annual Review of Plant Biology - Volume 64, 2013

Presented is a historical perspective of one scientist's journey from war-torn Europe to the opportunities presented by a flexible US educational system. It celebrates the opening of the science establishment that began in the 1950s and its fostering of basic research, and recognizes individuals who were instrumental in guiding the author's education as well as those with whom she later participated in collaborative algal plant research. The initial discovery and later elucidation of phycobilisome structure are elaborated, including the structural connection with photosystem II. Furthermore, she summarizes some of her laboratory's results on carotenoids and its exploration of the isoprenoid pathway in cyanobacteria. Finally, she comments on the gender gap and how her generation benefited when opportunities for women scientists were enlarged.

Chronic disease is a major social challenge of the twenty-first century. In this review, we examine the evidence for discordance between modern diets and those on which humankind evolved as the cause of the increasing incidence of chronic diseases, and the evidence supporting consumption of plant foods as a way to reduce the risk of chronic disease. We also examine the evidence for avoiding certain components of plant-based foods that are enriched in Western diets, and review the mechanisms by which different phytonutrients are thought to reduce the risk of chronic disease. This body of evidence strongly suggests that consuming more fruits and vegetables could contribute both to medical nutrition therapies, as part of a package of treatments for conditions like type 2 diabetes, heart disease, cancer, and obesity, and to the prevention of these diseases. Plant science should be directed toward improving the quality of plant-based foods by building on our improved understanding of the complex relationships between plants, our diet, and our health.

Human selection during crop domestication has resulted in remarkable transformations of plant phenotypes, providing a window into the genetic basis of morphological evolution. Recent progress in our understanding of the genetic architecture of novel plant traits has emerged from combining advanced molecular technologies with improved experimental designs, including nested association mapping, genome-wide association studies, population genetic screens for signatures of selection, and candidate gene approaches. These studies reveal a diversity of underlying causative mutations affecting phenotypes important in plant domestication and crop improvement, including coding sequence substitutions, presence/absence and copy number variation, transposon activation leading to novel gene structures and expression patterns, diversification following gene duplication, and polyploidy leading to altered combinatorial capabilities. The genomic regions unknowingly targeted by human selection include both structural and regulatory genes, often with results that propagate through the transcriptome as well as to other levels in the biosynthetic and morphogenetic networks.

Although heterosis, or hybrid vigor, is widely exploited in agriculture, a complete description of its molecular underpinnings has remained elusive despite extensive investigation. It appears that there is not a single, simple explanation for heterosis. Instead, it is likely that heterosis arises in crosses between genetically distinct individuals as a result of a diversity of mechanisms. Heterosis generally results from the action of multiple loci, and different loci affect heterosis for different traits and in different hybrids. Hence, multigene models are likely to prove most informative for understanding heterosis. Complementation of allelic variation, as well as complementation of variation in gene content and gene expression patterns, is likely to be an important contributor to heterosis. Epigenetic variation has the potential to interact in hybrid genotypes via novel mechanisms. Several other intriguing hypotheses are also under investigation. In crops, heterosis must be considered within the context of the genomic impacts of prior selection for agronomic traits.

Genomics is enabling a renaissance in all disciplines of plant biology. However, many plant genomes are complex and remain recalcitrant to current genomic technologies. The complexities of these nonmodel plant genomes are attributable to gene and genome duplication, heterozygosity, ploidy, and/or repetitive sequences. Methods are available to simplify the genome and reduce these barriers, including inbreeding and genome reduction, making these species amenable to current sequencing and assembly methods. Some, but not all, of the complexities in nonmodel genomes can be bypassed by sequencing the transcriptome rather than the genome. Additionally, comparative genomics approaches, which leverage phylogenetic relatedness, can aid in the interpretation of complex genomes. Although there are limitations in accessing complex nonmodel plant genomes using current sequencing technologies, genome manipulation and resourceful analyses can allow access to even the most recalcitrant plant genomes.

Reproductive isolation is both an indicator of speciation and a mechanism for maintaining species identity. Here we review the progress in studies of hybrid sterility in rice to illustrate the present understanding of the molecular and evolutionary mechanisms underlying reproductive isolation. Findings from molecular characterization of genes controlling hybrid sterility can be summarized with three evolutionary genetic models. The parallel divergence model features duplicated loci generated by genome evolution; in this model, the gametes abort when the two copies of loss-of-function mutants meet in hybrids. In the sequential divergence model, mutations of two linked loci occur sequentially in one lineage, and negative interaction between the ancestral and nascent alleles of different genes causes incompatibility. The parallel-sequential divergence model involves three tightly linked loci, exemplified by a killer–protector system formed of mutations in two steps. We discuss the significance of such findings and their implications for crop improvement.

Regulatory small RNAs, which range in size from 20 to 24 nucleotides, are ubiquitous components of endogenous plant transcriptomes, as well as common responses to exogenous viral infections and introduced double-stranded RNA (dsRNA). Endogenous small RNAs derive from the processing of helical RNA precursors and can be categorized into several groups based on differences in biogenesis and function. A major distinction can be observed between small RNAs derived from single-stranded precursors with a hairpin structure [referred to here as hairpin RNAs (hpRNAs)] and those derived from dsRNA precursors [small interfering RNAs (siRNAs)]. hpRNAs in plants can be divided into two secondary groups: microRNAs and those that are not microRNAs. The currently known siRNAs fall mostly into one of three secondary groups: heterochromatic siRNAs, secondary siRNAs, and natural antisense transcript siRNAs. Tertiary subdivisions can be identified within many of the secondary classifications as well. Comparisons between the different classes of plant small RNAs help to illuminate key goals for future research.

Protein-protein interactions are a critical element of biological systems, and the analysis of interaction partners can provide valuable hints about unknown functions of a protein. In recent years, several large-scale protein interaction studies have begun to unravel the complex networks through which plant proteins exert their functions. Two major classes of experimental approaches are used for protein interaction mapping: analysis of direct interactions using binary methods such as yeast two-hybrid or split ubiquitin, and analysis of protein complexes through affinity purification followed by mass spectrometry. In addition, bioinformatics predictions can suggest interactions that have evaded detection by other methods or those of proteins that have not been investigated. Here we review the major approaches to construct, analyze, use, and carry out quality control on plant protein interactome networks. We present experimental and computational approaches for large-scale mapping, methods for validation or smaller-scale functional studies, important bioinformatics resources, and findings from recently published large-scale plant interactome network maps.

Seeds develop differently in dicots and monocots, especially with respect to the major storage organs. High-resolution transcriptome data have provided the first insights into the molecular networks and pathway interactions that function during the development of individual seed compartments. Here, we review mainly recent data obtained by systems biology–based approaches, which have allowed researchers to construct and model complex metabolic networks and fluxes and identify key limiting steps in seed development. Comparative coexpression network analyses define evolutionarily conservative (FUS3/ABI3/LEC1) and divergent (LEC2) networks in dicots and monocots. Finally, we discuss the determination of seed size—an important yield-related characteristic—as mediated by a number of processes (maternal and epigenetic factors, fine-tuned regulation of cell death in distinct seed compartments, and endosperm growth) and underlying genes defined through mutant analyses. Altogether, systems approaches can make important contributions toward a more complete and holistic knowledge of seed biology and thus support strategies for knowledge-based molecular breeding.

Fruiting structures in the angiosperms range from completely dry to highly fleshy organs and provide many of our major crop products, including grains. In the model plant Arabidopsis, which has dry fruits, a high-level regulatory network of transcription factors controlling fruit development has been revealed. Studies on rare nonripening mutations in tomato, a model for fleshy fruits, have provided new insights into the networks responsible for the control of ripening. It is apparent that there are strong similarities between dry and fleshy fruits in the molecular circuits governing development and maturation. Translation of information from tomato to other fleshy-fruited species indicates that regulatory networks are conserved across a wide spectrum of angiosperm fruit morphologies. Fruits are an essential part of the human diet, and recent developments in the sequencing of angiosperm genomes have provided the foundation for a step change in crop improvement through the understanding and harnessing of genome-wide genetic and epigenetic variation.

Tip growth is employed throughout the plant kingdom. Our understanding of tip growth has benefited from modern tools in molecular genetics, which have enabled the functional characterization of proteins mediating tip growth. Here we first discuss the evolutionary role of tip growth in land plants and then describe the prominent model tip-growth systems, elaborating on some advantages and disadvantages of each. Next we review the organization of tip-growing cells, the role of the cytoskeleton, and recent developments concerning the physiological basis of tip growth. Finally, we review advances in the understanding of the extracellular signals that are known to guide tip-growing cells.

With increasing demand to support and accelerate progress in breeding for novel traits, the plant research community faces the need to accurately measure increasingly large numbers of plants and plant parameters. The goal is to provide quantitative analyses of plant structure and function relevant for traits that help plants better adapt to low-input agriculture and resource-limited environments. We provide an overview of the inherently multidisciplinary research in plant phenotyping, focusing on traits that will assist in selecting genotypes with increased resource use efficiency. We highlight opportunities and challenges for integrating noninvasive or minimally invasive technologies into screening protocols to characterize plant responses to environmental challenges for both controlled and field experimentation. Although technology evolves rapidly, parallel efforts are still required because large-scale phenotyping demands accurate reporting of at least a minimum set of information concerning experimental protocols, data management schemas, and integration with modeling. The journey toward systematic plant phenotyping has only just begun.

The expression of nuclear protein-coding genes is controlled by dynamic mechanisms ranging from DNA methylation, chromatin modification, and gene transcription to mRNA maturation, turnover, and translation and the posttranslational control of protein function. A genome-scale assessment of the spatiotemporal regulation of gene expression is essential for a comprehensive understanding of gene regulatory networks. However, there are major obstacles to the precise evaluation of gene regulation in multicellular plant organs; these include the monitoring of regulatory processes at levels other than steady-state transcript abundance, resolution of gene regulation in individual cells or cell types, and effective assessment of transient gene activity manifested during development or in response to external cues. This review surveys the advantages and applications of microgenomics technologies that enable panoramic quantitation of cell-type-specific expression in plants, focusing on the importance of querying gene activity at multiple steps in the continuum, from histone modification to selective translation.

Recent advances in genome engineering provide newfound control over a plant's genetic material. It is now possible for most bench scientists to alter DNA in living plant cells in a variety of ways, including introducing specific nucleotide substitutions in a gene that change a protein's amino acid sequence, deleting genes or chromosomal segments, and inserting foreign DNA at precise genomic locations. Such targeted DNA sequence modifications are enabled by sequence-specific nucleases that create double-strand breaks in the genomic loci to be altered. The repair of the breaks, through either homologous recombination or nonhomologous end joining, can be controlled to achieve the desired sequence modification. Genome engineering promises to advance basic plant research by linking DNA sequences to biological function. Further, genome engineering will enable plants' biosynthetic capacity to be harnessed to produce the many agricultural products required by an expanding world population.

The advent of fluorescent proteins and access to modern imaging technologies have dramatically accelerated the pace of discovery in plant cell biology. Remarkable new insights into such diverse areas as plant pathogenesis, cytoskeletal dynamics, sugar transport, cell wall synthesis, secretory control, and hormone signaling have come from careful examination of living cells using advanced optical probes. New technologies, both commercially available and on the horizon, promise a continued march toward more quantitative methods for imaging and for extending the optical exploration of biological structure and activity to molecular scales. In this review, we lay out fundamental issues in imaging plant specimens and look ahead to several technological innovations in molecular tools, instrumentation, imaging methods, and specimen handling that show promise for shaping the coming era of plant cell biology.

Extensive studies in both lower and higher plants indicate that plant phytochrome photoreceptors signal not only by regulating transcription in the nucleus but also by acting within the cytoplasm, the latter signaling routes acting within minutes or even seconds and also providing directional information. Directional signals seem to arise from phytochromes attached anisotropically to the plasma membrane. Neochromes—phytochrome-phototropin hybrid photoreceptors probably attached to the plasma membrane—provide this signal in various ferns and perhaps certain algae but are absent from other groups. In mosses and probably higher plants too, a subpopulation of canonical phytochromes interact with phototropins at the plasma membrane and thereby steer directional responses. Phytochromes also seem able to regulate translation in the cytoplasm. This review discusses putative phytochrome functions in these contexts.

The dynamic light environment of vegetation canopies is perceived by phytochromes, cryptochromes, phototropins, and UV RESISTANCE LOCUS 8 (UVR8). These receptors control avoidance responses to preclude exposure to limiting or excessive light and acclimation responses to cope with conditions that cannot be avoided. The low red/far-red ratios of shade light reduce phytochrome B activity, which allows PHYTOCHROME INTERACTING FACTORS (PIFs) to directly activate the transcription of auxin-synthesis genes, leading to shade-avoidance responses. Direct PIF interaction with DELLA proteins links gibberellin and brassinosteroid signaling to shade avoidance. Shade avoidance also requires CONSTITUTIVE PHOTOMORPHOGENESIS 1 (COP1), a target of cryptochromes, phytochromes, and UVR8. Multiple regulatory loops and the input of the circadian clock create a complex network able to respond even to subtle threats of competition with neighbors while still compensating for major environmental fluctuations such as the day-night cycles.

Nonenzymatic lipid oxidation is usually viewed as deleterious. But if this is the case, then why does it occur so frequently in cells? Here we review the mechanisms of membrane peroxidation and examine the genesis of reactive electrophile species (RES). Recent evidence suggests that during stress, both lipid peroxidation and RES generation can benefit cells. New results from genetic approaches support a model in which entire membranes can act as supramolecular sinks for singlet oxygen, the predominant reactive oxygen species (ROS) in plastids. RES reprogram gene expression through a class II TGA transcription factor module as well as other, unknown signaling pathways. We propose a framework to explain how RES signaling promotes cell “REScue” by stimulating the expression of genes encoding detoxification functions, cell cycle regulators, and chaperones. The majority of the known biological activities of oxygenated lipids (oxylipins) in plants are mediated either by jasmonate perception or through RES signaling networks.

As one of the most important mineral nutrient elements, potassium (K⁺) participates in many plant physiological processes and determines the yield and quality of crop production. In this review, we summarize K⁺ signaling processes and K⁺ transport regulation in higher plants, especially in plant responses to K⁺-deficiency stress. Plants perceive external K⁺ fluctuations and generate the initial K⁺ signal in root cells. This signal is transduced into the cytoplasm and encoded as Ca²⁺ and reactive oxygen species signaling. K⁺-deficiency-induced signals are subsequently decoded by cytoplasmic sensors, which regulate the downstream transcriptional and posttranslational responses. Eventually, plants produce a series of adaptive events in both physiological and morphological alterations that help them survive K⁺ deficiency.

Endoplasmic reticulum (ER) stress is of considerable interest to plant biologists because it occurs in plants subjected to adverse environmental conditions. ER stress responses mitigate the damage caused by stress and confer levels of stress tolerance to plants. ER stress is activated by misfolded proteins that accumulate in the ER under adverse environmental conditions. Under these conditions, the demand for protein folding exceeds the capacity of the system, which sets off the unfolded protein response (UPR). Two arms of the UPR signaling pathway have been described in plants: one that involves two ER membrane–associated transcription factors (bZIP17 and bZIP28) and another that involves a dual protein kinase (RNA-splicing factor IRE1) and its target RNA (bZIP60). Under mild or short-term stress conditions, signaling from IRE1 activates autophagy, a cell survival response. But under severe or chronic stress conditions, ER stress can lead to cell death.